Polyploidy, which results in the presence of more than two sets of homologous chromosomes represents a major feature of plant genomes that have undergone successive rounds of duplication followed by more or less rapid diploidization during their evolutionary history. Polyploid complexes containing diploid and derived polyploid taxa are excellent model systems for understanding the short-term consequences of whole genome duplication, and have been particularly well-explored in evolutionary ecology (Ramsey and Ramsey 2014, Rice et al. 2019). Many polyploids (especially when resulting from interspecific hybridization, i.e. allopolyploids) are successful invaders (te Beest et al. 2012) as a result of rapid genome dynamics, functional novelty, and trait evolution. The origin (parental legacy) and modes of formation of polyploids have a critical impact on the subsequent polyploid evolution. Thus, elucidation of the genomic composition of polyploids is fundamental to understanding trait evolution, and such knowledge is still lacking for many invasive species.

Genus Ludwigia is characterized by a complex taxonomy, with an underexplored evolutionary history. Species from section Jussieae form a polyploid complex with diploids, tetraploids, hexaploids, and decaploids that are notorious invaders in freshwater and riparian ecosystems (Thouvenot et al.2013).   Molecular phylogeny of the genus based on nuclear and chloroplast sequences (Liu et al. 2027) suggested some relationships between diploid and polyploid species, without fully resolving the question of the parentage of the polyploids. In their study, Barloy et al. (2023) have used a combination of molecular cytogenetics (Genomic In situ Hybridization), morphology and experimental crosses to elucidate the genomic compositions of the polyploid species, and show that the examined polyploids are of hybrid origin (allopolyploids). The tetraploid L. stolonifera derives from the diploids L. peploides subsp. montevidensis (AA genome) and L. helminthorhiza (BB genome). The tetraploid L. ascendens also share the BB genome combined with an undetermined different genome. The hexaploid L. grandiflora subsp. grandiflora has inherited the diploid AA genome combined with additional unidentified genomes. The decaploid L. grandiflora subsp. hexapetala has inherited the tetraploid L. stolonifera and the hexaploid L. grandiflora subsp. hexapetala genomes. As the authors point out, further work is needed, including additional related diploid (e.g. other subspecies of L. peploides) or tetraploid (L.  hookeri and L. peduncularis)  taxa that remain to be investigated, to address the nature of the undetermined parental genomes mentioned above. 

The presented work (Barloy et al.  2023) provides significant knowledge of this poorly investigated group with regard to genomic information and polyploid origin, and opens perspectives for future studies. The authors also detect additional diagnostic morphological traits of interest for in-situ discrimination of the taxa when monitoring invasive populations.  

References

Barloy D., Portillo-Lemus L., Krueger-Hadfield S.A., Huteau V., Coriton O. (2024). Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of molecular cytogenetic, morphological, and crossing investigations. BioRxiv, ver. 4 peer-reviewed and recommended  by Peer Community in Evolutionary Biology https://doi.org/10.1101/2023.01.02.522458

te Beest M., Le Roux J.J., Richardson D.M., Brysting A.K., Suda J., Kubešová M., Pyšek P. (2012). The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany, Volume 109, Issue 1 Pages 19–45, https://doi.org/10.1093/aob/mcr277

Ramsey J. and Ramsey T. S. (2014). Ecological studies of polyploidy in the 100 years following its discovery Phil. Trans. R. Soc. B369 1–20  https://doi.org/10.1098/rstb.2013.0352  

Rice, A., Šmarda, P., Novosolov, M. et al. (2019). The global biogeography of polyploid plants. Nat Ecol Evol 3, 265–273. https://doi.org/10.1038/s41559-018-0787-9

Thouvenot L, Haury J, Thiebaut G. (2013). A success story: Water primroses, aquatic plant pests. Aquat. Conserv. Mar. Freshw. Ecosyst. 23:790–803  https://doi.org/10.1002/aqc.2387  

Spatial genetic structure, i.e. the non-random spatial distribution of genotypes, arises in populations because of different processes including spatially limited dispersal and selection. Knowledge on the spatial genetic structure of plant populations is important to assess biological parameters such as gene dispersal distances and the potential for local adaptations, as well as for applications in conservation management and breeding. In their work, Niskanen and colleagues demonstrate a multifaceted approach to characterise the spatial genetic structure in two replicate sites of a continuously distributed Scots pine population in South-Eastern Finland. They mapped and assessed the ages of 469 naturally regenerated adults and genotyped them using a SNP array which resulted in 157 325 filtered polymorphic SNPs. Their dataset is remarkably powerful because of the large numbers of both individuals and SNPs genotyped. This made it possible to characterise precisely the decay of genetic relatedness between individuals with spatial distance despite the extensive dispersal capacity of Scots pine through pollen, and ensuing expectations of an almost panmictic population.

The authors’ data analysis was particularly thorough. They demonstrated that two metrics of pairwise relatedness, the genomic relationship matrix (GRM, Yang et al. 2011) and the kinship coefficient (Loiselle et al. 1995) were strongly correlated and produced very similar inference of family relationships: >99% of pairs of individuals were unrelated, and the remainder exhibited 2nd (e.g., half-siblings) to 4th degree relatedness. Pairwise relatedness decayed with spatial distance which resulted in extremely weak but statistically significant spatial genetic structure in both sites, quantified as Sp=0.0005 and Sp=0.0008. These estimates are at least an order of magnitude lower than estimates in the literature obtained in more fragmented populations of the same species or in other conifers. Estimates of the neighbourhood size, the effective number of potentially mating individuals belonging to a within-population neighbourhood (Wright 1946), were relatively large with Nb=1680-3210 despite relatively short gene dispersal distances, σg = 36.5–71.3m, which illustrates the high effective density of the population. 

The authors showed the implications of their findings for selection. The capacity for local adaptation depends on dispersal distances and the strength of the selection coefficient. In the study population, the authors inferred that local adaptation can only occur if environmental heterogeneity occurs over a distance larger than approximately one kilometre (or larger, if considering long-distance dispersal). Interestingly, in Scots pine, no local adaptation has been described on similar geographic scales, in contrast to some other European or Mediterranean conifers (Scotti et al. 2023).

The authors’ results are relevant for the management of conservation and breeding. They showed that related individuals occurred within sites only and that they shared a higher number of rare alleles than unrelated ones. Since rare alleles are enriched in new and recessive deleterious variants, selecting related individuals could have negative consequences in breeding programmes. The authors also showed, in their response to reviewers, that their powerful dataset was not suitable to obtain a robust estimate of effective population size, Ne, based on the linkage disequilibrium method (Do et al. 2014). This illustrated that the estimation of Ne used for genetic indicators supported in international conservation policy (Hoban et al. 2020, CBD 2022) remains challenging in large and continuous populations (see also Santo-del-Blanco et al. 2023, Gargiulo et al. 2024).

References

CBD (2022) Kunming-Montreal Global Biodiversity Framework. https://www.cbd.int/doc/decisions/cop-15/cop-15-dec-04-en.pdf

Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014). NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne ) from genetic data. Molecular Ecology Resources 14: 209–214. https://doi.org/10.1111/1755-0998.12157

Gargiulo R, Decroocq V, González-Martínez SC, Paz-Vinas I, Aury JM, Kupin IL, Plomion C, Schmitt S, Scotti I, Heuertz M (2024) Estimation of contemporary effective population size in plant populations: limitations of genomic datasets. Evolutionary Applications, in press, https://doi.org/10.1101/2023.07.18.549323

Hoban S, Bruford M, D’Urban Jackson J, Lopes-Fernandes M, Heuertz M, Hohenlohe PA, Paz-Vinas I, et al. (2020) Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved. Biological Conservation 248: 108654. https://doi.org/10.1016/j.biocon.2020.108654

Loiselle BA, Sork VL, Nason J & Graham C (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 82: 1420–1425. https://doi.org/10.1002/j.1537-2197.1995.tb12679.x

Santos-del-Blanco L, Olsson S, Budde KB, Grivet D, González-Martínez SC, Alía R, Robledo-Arnuncio JJ (2022). On the feasibility of estimating contemporary effective population size (Ne) for genetic conservation and monitoring of forest trees. Biological Conservation 273: 109704. https://doi.org/10.1016/j.biocon.2022.109704

Scotti I, Lalagüe H, Oddou-Muratorio S, Scotti-Saintagne C, Ruiz Daniels R, Grivet D, et al. (2023) Common microgeographical selection patterns revealed in four European conifers. Molecular Ecology 32: 393-411. https://doi.org/10.1111/mec.16750

Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31: 39–59. https://doi.org/10.1093/genetics/31.1.39

Yang J, Lee SH, Goddard ME & Visscher PM (2011) GCTA: a tool for genome-wide complex trait analysis. The American Journal of Human Genetics 88: 76–82. https://www.cell.com/ajhg/pdf/S0002-9297(10)00598-7.pdf